Joost Vanoverbeke

Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization

Empirical population genetic studies have been dominated by a neutralist view, according to which gene flow and drift are the main forces driving population genetic structure in nature. The neutralist view in essence describes a process of isolation by dispersal limitation (IBDL) that generally leads to a pattern of isolation by distance (IBD). Recently, however, conceptual frameworks have been put forward that view local genetic adaptation as an important driver of population genetic structure. Isolation by adaptation (IBA) and monopolization (M) posit that gene flow among natural populations is reduced as a consequence of local genetic adaptation. IBA stresses that effective gene flow is reduced among habitats that show dissimilar ecological characteristics, leading to a pattern of isolation by environment. In monopolization, local genetic adaptation of initial colonizing genotypes results in a reduction in gene flow that fosters the persistence of founder effects. Here, we relate these different processes driving landscape genetic structure to patterns of IBD and isolation by environment (IBE). We propose a method to detect whether IBDL, IBA and M shape genetic differentiation in natural landscapes by studying patterns of variation at neutral and non‐neutral markers as well as at ecologically relevant traits. Finally, we reinterpret a representative number of studies from the recent literature by associating patterns to processes and identify patterns associated with local genetic adaptation to be as common as IBDL in structuring regional genetic variation of populations in the wild. Our results point to the importance of quantifying environmental gradients and incorporating ecology in the analysis of population genetics.

Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna.

Provided that gene flow is not too high, selection by local environmental conditions in heterogeneous landscapes can lead to genetic adaptation of natural populations to their local habitat. Pollution with anthropogenic toxicants may create pronounced environmental gradients that impose strong local selection pressures. Toxic contaminants may also directly impact genetic structure in natural populations by exhibiting genotoxicity or by causing population declines resulting in genetic bottlenecks. Using populations of Daphnia magna established from the dormant egg banks of ponds located in a landscape dominated by anthropogenic impact, we aimed at detecting evidence for local adaptation to environmental contamination. We explored the relationship between land use around the 10 investigated ponds, population genetic diversity as measured by neutral genetic markers (polymorphic allozymes) and the tolerance of the populations originating from these ponds to acute lethal effects of two model toxicants, the pesticide carbaryl and the metal potassium dichromate. Genetic diversity of the populations as observed by neutral markers tended to be negatively impacted by agricultural land use intensity (Spearman rank correlation, R=-0.614, P=0.059), indicating that genetic bottlenecks may have resulted from anthropogenic impact. We experimentally observed differences in susceptibility to both carbaryl and potassium dichromate among the studied pond populations of D. magna (analysis of deviance, P<0.001). Because the experimental design excluded the possibility of physiological adaptation of the test animals to the toxicants, we conclude that the differences in susceptibility must have a genetic basis. Moreover, carbaryl tolerance levels of the populations tended to increase with increasing agricultural land use intensity as described by ranked percentage of land coverage with cereal and corn crop in the proximity of the ponds (Spearman rank correlation, R=0.602, P=0.066). Together, these two findings provide evidence for local adaptation of D. magna populations to pesticide contamination. Overall, the results demonstrate the potential selection pressure imposed by anthropogenic pollution and provide evidence that genetic erosion in natural Daphnia populations is related to anthropogenic impact.

A crucial step toward realism: responses to climate change from an evolving metacommunity perspective

We need to understand joint ecological and evolutionary responses to climate change to predict future threats to biological diversity. The ‘evolving metacommunity’ framework emphasizes that interactions between ecological and evolutionary mechanisms at both local and regional scales will drive community dynamics during climate change. Theory suggests that ecological and evolutionary dynamics often interact to produce outcomes different from those predicted based on either mechanism alone. We highlight two of these dynamics: (i) species interactions prevent adaptation of nonresident species to new niches and (ii) resident species adapt to changing climates and thereby prevent colonization by nonresident species. The rate of environmental change, level of genetic variation, source‐sink structure, and dispersal rates mediate between these potential outcomes. Future models should evaluate multiple species, species interactions other than competition, and multiple traits. Future experiments should manipulate factors such as genetic variation and dispersal to determine their joint effects on responses to climate change. Currently, we know much more about how climates will change across the globe than about how species will respond to these changes despite the profound effects these changes will have on global biological diversity. Integrating evolving metacommunity perspectives into climate change biology should produce more accurate predictions about future changes to species distributions and extinction threats.

Among-populational genetic differentiation in the cyclical parthenogen Daphnia magna (Crustacea, Anomopoda) and its relation to geographic distance and clonal diversity

Using allozyme data based on four polymorphic enzymeloci, we present an analysis of geneticdifferentiation among eight Daphnia magnapopulations, separated by less than 100 m to more than500 km from each other. In spite of the large range ofgeographic distances, there was only a slight tendencyfor an increase in genetic differentiation withincreasing geographic distance between populations,and the relation was not significant. This was mainlydue to the fact that neighbouring populations werealready highly genetically differentiated. Our resultssuggest that in populations in which only a fewabundant clones are present after a period of strongclonal selection, among-populational geneticdifferentiation as revealed by allozyme markers isinflated as a result of stochasticity involving chanceassociations of alleles with specific abundantgenotypes. Indices quantifying genetic differentiationwere much higher among populations with a low clonaldiversity than among populations with a high clonaldiversity.

Genetic structure of cyclic parthenogenetic zooplankton populations - : a conceptual framework

The genetic structure of cyclic parthenogenetic zooplankton populations is strongly determined by the consequences of combining sexual and asexual reproduction in the same life cycle. Since the pioneering population genetic studies on freshwater zooplankton in the 1970s, a distinction has been made between the genetic structure of permanent and intermittent populations. However, the results of many studies do not fit the expectations of this dichotomous model, for example when large lake populations are considered. In this paper, we present a unifying framework for understanding the genetic structure of cyclic parthenogenetic zooplankton populations, focusing on three factors that determine their degree of clonality and within-population genetic diversity as well as their among-population genetic differentiation: the size of the dormant egg bank, length of the growing season, and strength of clonal selection. We illustrate the importance of each of these factors, and show that our broader concept better explains the variation in genetic structure observed in natural populations of cyclic parthenogens than the earlier implicitly dichotomous model.

Evolving Perspectives on Monopolization and Priority Effects

Biologists are often confronted with high levels of unexplained variation when studying the processes that determine genetic and species diversity. Here, we argue that eco-evolutionary interactions might often play an important role during colonization and have longstanding effects on populations and communities. Adaptation following colonization can produce a strong positive feedback loop that promotes priority effects and context-dependent trajectories of population or species assembly. We establish how monopolization, and more generally evolution-mediated priority effects, influence ecological patterns at multiple scales of space, time, and biological organization. We then highlight the underappreciated implications for our understanding of population and landscape genetics, adaptive evolution, community diversity, biogeography, and conservation biology. We indicate multiple future directions for research, including extending theory beyond competition.

EXTINCTION, RECOLONIZATION, AND DISPERSAL THROUGH TIME IN A PLANKTONIC CRUSTACEAN

Dormant propagule banks are important reservoirs of biological and genetic diversity of local communities and populations and provide buffering mechanisms against extinction. Although dormant stages of various plant and animal species are known to remain viable for decades and even centuries, little is known about the effective influence of recolonization from such old sources on the genetic continuity of intermittent populations under natural conditions. Using recent and old dormant eggs recovered from a dated lake sediment core in Kenya, we traced the genetic composition of a local population of the planktonic crustacean Daphnia barbata through a sequence of extinction and recolonization events. This was combined with a phylogeographic and population-genetic survey of regional populations. Four successive populations, fully separated in time, inhabited Lake Naivasha from ca. 1330 to 1570 AD, from ca. 1610 to 1720 AD, from ca. 1840 to 1940 AD, and from 1995 to the present (2001 AD). Our results strongly indicate genetic continuity between the 1840-1940 and 1995-2001 populations, which are separated in time by at least 50 years, and close genetic relatedness of them both to the 1330-1580 population. A software tool (Colonize) was developed to find the most likely source population of the refounded 1995-2001 population and to test the number of colonists involved in the recolonization event. The results confirmed that the 1995-2001 population most probably developed out of a limited number of surviving local dormant eggs from the previous population, rather than out of individuals from regional (central and southern Kenya) or more distant (Ethiopia, Zimbabwe) populations that may have immigrated to Lake Naivasha through passive dispersal. These results emphasize the importance of prolonged dormancy for the natural long-term dynamics of crustacean zooplankton in fluctuating environments and suggest an important role of old local dormant egg banks in aquatic habitat restoration.

Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia

Toxic algal blooms are an important problem worldwide. The literature on toxic cyanobacteria blooms in inland waters reports widely divergent results on whether zooplankton can control cyanobacteria blooms or cyanobacteria suppress zooplankton by their toxins. Here we test whether this may be due to genotype × genotype interactions, in which interactions between the large‐bodied and efficient grazer Daphnia and the widespread cyanobacterium Microcystis are not only dependent on Microcystis strain or Daphnia genotype but are specific to genotype × genotype combinations. We show that genotype × genotype interactions are important in explaining mortality in short‐time exposures of Daphnia to Microcystis. These genotype × genotype interactions may result in local coadaptation and a geographic mosaic of coevolution. Genotype × genotype interactions can explain why the literature on zooplankton–cyanobacteria interactions is seemingly inconsistent, and provide hope that zooplankton can contribute to the suppression of cyanobacteria blooms in restoration projects.

Low historical rates of cuckoldry in a Western European human population traced by Y-chromosome and genealogical data

Recent evidence suggests that seeking out extra-pair paternity (EPP) can be a viable alternative reproductive strategy for both males and females in many pair-bonded species, including humans. Accurate data on EPP rates in humans, however, are scant and mostly restricted to extant populations. Here, we provide the first large-scale, unbiased genetic study of historical EPP rates in a Western European human population based on combining Y-chromosomal data to infer genetic patrilineages with genealogical and surname data, which reflect known historical presumed paternity. Using two independent methods, we estimate that over the last few centuries, EPP rates in Flanders (Belgium) were only around 1–2% per generation. This figure is substantially lower than the 8–30% per generation reported in some behavioural studies on historical EPP rates, but comparable with the rates reported by other genetic studies of contemporary Western European populations. These results suggest that human EPP rates have not changed substantially during the last 400 years in Flanders and imply that legal genealogies rarely differ from the biological ones. This result has significant implications for a diverse set of fields, including human population genetics, historical demography, forensic science and human sociobiology.

Clonal erosion and genetic drift in cyclical parthenogens--the interplay between neutral and selective processes.

The occurrence of alternating phases of clonal and sexual reproduction may strongly impact the interplay between neutral and selective genetic variation in populations. Using a physiologically structured model of the life history of Daphnia, we investigated to what extent clonal erosion associated with selection during the clonal phase affects the genetic structure as observed by neutral markers. Incorporating conservative levels of quantitative genetic variation at 11 physiological and life history traits induces strong clonal erosion, reducing clonal diversity (CD) near the end of the simulations (1000 days) to a level between 1 and 5, even in habitats with high initial CD (108 clones). This strong clonal erosion caused by selection can result in reduced genetic diversity, significant excess of heterozygotes and significant genetic differentiation between populations as observed by neutral markers. Our results indicate that, especially in relatively small habitats, clonal selection may strongly impact the genetic structure and may contribute to the often observed high level of neutral genetic differentiation among natural populations of cyclical parthenogens.